Multiple origins of Indian dwarf wheat by mutations targeting the TREE domain of a GSK3-like kinase for drought tolerance, phosphate uptake, and grain quality.

KEY MESSAGE: Multiple origins of Indian dwarf wheat were due to two mutations targeting the same TREE domain of a GSK3-like kinase, and these mutations confer to enhanced drought tolerance and increased phosphate and nitrogen accumulation for adaptation to the dry climate of Indian and Pakistan. Indian dwarf wheat, featured by the short stature, erect leaves, dense spikes, and small, spherical grains, was a staple crop in India and Pakistan from the Bronze Age until the early 1900s. These morphological features are controlled by a single locus Sphaerococcum 1 (S1), but the genetic identity of the locus and molecular mechanisms underlying the selection of this wheat type are unknown. In this study, we showed that the origin of Indian dwarf wheat was due to two independent missense mutations targeting the conserved TREE domain of a GSK3-like kinase, which is homologous to the Arabidopsis BIN2 protein, a negative regulator in brassinosteroid signaling. The S1 protein is involved in brassinosteroid signaling by physical interaction with the wheat BES1/BZR1 proteins. The dwarf alleles are insensitive to brassinosteroid, upregulates brassinosteroid biosynthetic genes, significantly enhanced drought tolerance, facilitated phosphate accumulation, and increased high molecular weight glutenins. It is the enhanced drought tolerance and accumulation of nitrogen and phosphate that contributed to the adaptation of such a small-grain form of wheat to the dry climate of India and Pakistan. Thus, our research not only identified the genetic events underlying the origin of the Indian dwarf wheat, but also revealed the function of brassinosteroid in the regulation of drought tolerance, phosphate homeostasis, and grain quality.